Photosynthetic electron transport in the bundle sheath of maize

Leegood, Richard C.; Crowther, David; Walker, David A.; Hínd, Geoffrey

doi:10.1016/0014-5793(81)81040-x

“…On the other hand, bundle-sheath chloroplasts have to generate ATP for CO2 fixation via the Calvin-Benson cycle and it has been shown that this ATP demand is fulfilled by cyclic electron transport (Chapman et al 1980;Leegood et al 1981). Thus, if the NAD(P)H dehydrogenase is an essential component of the cyclic electron-transport pathway in plastids, one may expect that the relative amount of the enzyme is increased in bundle-sheath chloroplasts as compared to mesophyll chloroplasts.…”

Section: Introductionmentioning

confidence: 96%

Differential expression of plastome-encoded ndh genes in mesophyll and bundle-sheath chloroplasts of the C4 plant Sorghum bicolor indicates that the complex I-homologous NAD(P)H-plastoquinone oxidoreductase is involved in cyclic electron transport

Kubicki

¹

,

Funk

²

,

Westhoff

³

et al. 1996

Planta

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Abstract. Cyanobacteria and plastids harbor a putative NAD(P)H-or ferredoxin-plastoquinone oxidoreductase that is homologous to the NADH-ubiquinone oxidoreductase (complex I) of mitochondria and eubacteria. The enzyme is a multimeric protein complex that consists of at least 11 subunits (NDH-A-K) and is localized in the stroma lamellae of the thylakoid membrane system. We investigated the expression of the different subunits of the enzyme in mesophyll and bundle-sheath chloroplasts of Sorghum bicolor [L.] Moench, a C4 plant of the NADPmalic enzyme type. The relative amounts of the subunits NDH-H, -J and -K were strongly increased in bundlesheath plastids as compared to mesophyll plastids. This increase was accompanied by enhanced transcript levels for all subunits except NDH-I. Because the main function of the protein complexes in the thylakoid membranes of bundle-sheath chloroplasts (photosystem I, cytochrome b6/J:complex and ATPase) is the generation of ATP for C02 fixation via cyclic electron transport, we conclude that the NAD(P)H/ferredoxin-plastoquinone oxidoreductase is an essential component of the cyclic electrontransport pathway in chloroplasts.

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“…adaptation to salt stress conditions (Jeanjean et al, 1993). In the bundle sheath cell chloroplasts of C 4 plants, PS II is low or undetectable (Woo et al, 1970) and ATP supply is totally dependent upon PS I-mediated cyclic electron transport (Leegood et al, 1981).In C 3 plants, PS I-driven cyclic electron flow has been studied mainly in vitro on isolated chloroplasts or thylakoids with addition of artificial cofactors or reduced ferredoxin (Bendall and Manasse, 1995). Under those conditions, the redox poise was proposed to play an important role in the regulation of the rate of cyclic electron flow (Arnon and Chain, 1975; Heber et al, 1978; Fork and Herbert, 1993), with neither full reduction of the chloroplast electron transport chain (Ziem-Hanck and Heber, 1980) nor excessive oxidation allowing cyclic electron flow to occur in vitro.…”

mentioning

confidence: 99%

Cyclic Electron Flow around Photosystem I in C3 Plants. In Vivo Control by the Redox State of Chloroplasts and Involvement of the NADH-Dehydrogenase Complex

Joët

¹

2002

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Cyclic electron flow around photosystem (PS) I has been widely described in vitro in chloroplasts or thylakoids isolated from C 3 plant leaves, but its occurrence in vivo is still a matter of debate. Photoacoustic spectroscopy and kinetic spectrophotometry were used to analyze cyclic PS I activity in tobacco (Nicotiana tabacum cv Petit Havana) leaf discs illuminated with far-red light. Only a very weak activity was measured in air with both techniques. When leaf discs were placed in anaerobiosis, a high and rapid cyclic PS I activity was measured. The maximal energy storage in far-red light increased to 30% to 50%, and the half-time of the P 700 re-reduction in the dark decreased to around 400 ms; these values are comparable with those measured in cyanobacteria and C 4 plant leaves in aerobiosis. The stimulatory effect of anaerobiosis was mimicked by infiltrating leaves with inhibitors of mitochondrial respiration or of the chlororespiratory oxidase, therefore, showing that changes in the redox state of intersystem electron carriers tightly control the rate of PS I-driven cyclic electron flow in vivo. Measurements of energy storage at different modulation frequencies of far-red light showed that anaerobiosis-induced cyclic PS I activity in leaves of a tobacco mutant deficient in the plastid Ndh complex was kinetically different from that of the wild type, the cycle being slower in the former leaves. We conclude that the Ndh complex is required for rapid electron cycling around PS I.During oxygenic photosynthesis, photosystem (PS) II and PS I cooperate to achieve a linear electron flow from H 2 O to NADP ϩ and to generate a transmembrane proton gradient driving ATP synthesis. However, ATP can also be produced by the sole PS I through cyclic electron transfer reactions (Arnon, 1959). This mechanism enables the generation of a proton gradient across the thylakoid membrane without NADP reduction by rerouting electrons of reduced PS I acceptors toward the intersystem carriers. Cyclic and linear electron transfers share a common sequence of electron carriers, namely the plastoquinone (PQ) pool, cytochrome b 6 /f complex, and plastocyanin (for review, see Fork and Herbert, 1993; Bendall and Manasse, 1995). This alternative electron flow has been shown to occur in vivo in cyanobacteria (Carpentier et al., 1984), in algae (Maxwell and Biggins, 1976; Ravenel et al., 1994), and in bundle sheath cells of C 4 plants (Herbert et al., 1990; Asada et al., 1993). In cyanobacteria, cyclic electron flow around PS I has been shown to provide extra ATP for different cellular processes, e.g. adaptation to salt stress conditions (Jeanjean et al., 1993). In the bundle sheath cell chloroplasts of C 4 plants, PS II is low or undetectable (Woo et al., 1970) and ATP supply is totally dependent upon PS I-mediated cyclic electron transport (Leegood et al., 1981).In C 3 plants, PS I-driven cyclic electron flow has been studied mainly in vitro on isolated chloroplasts or thylakoids with addition of artificial cofactors or reduced ferredoxi...

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“…adaptation to salt stress conditions (Jeanjean et al, 1993). In the bundle sheath cell chloroplasts of C 4 plants, PS II is low or undetectable (Woo et al, 1970) and ATP supply is totally dependent upon PS I-mediated cyclic electron transport (Leegood et al, 1981).…”

mentioning

confidence: 99%

Cyclic Electron Flow around Photosystem I in C3Plants. In Vivo Control by the Redox State of Chloroplasts and Involvement of the NADH-Dehydrogenase Complex

Joët

¹

,

Cournac

²

,

Peltier

³

et al. 2002

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Cyclic electron flow around photosystem (PS) I has been widely described in vitro in chloroplasts or thylakoids isolated from C 3 plant leaves, but its occurrence in vivo is still a matter of debate. Photoacoustic spectroscopy and kinetic spectrophotometry were used to analyze cyclic PS I activity in tobacco (Nicotiana tabacum cv Petit Havana) leaf discs illuminated with far-red light. Only a very weak activity was measured in air with both techniques. When leaf discs were placed in anaerobiosis, a high and rapid cyclic PS I activity was measured. The maximal energy storage in far-red light increased to 30% to 50%, and the half-time of the P 700 re-reduction in the dark decreased to around 400 ms; these values are comparable with those measured in cyanobacteria and C 4 plant leaves in aerobiosis. The stimulatory effect of anaerobiosis was mimicked by infiltrating leaves with inhibitors of mitochondrial respiration or of the chlororespiratory oxidase, therefore, showing that changes in the redox state of intersystem electron carriers tightly control the rate of PS I-driven cyclic electron flow in vivo. Measurements of energy storage at different modulation frequencies of far-red light showed that anaerobiosis-induced cyclic PS I activity in leaves of a tobacco mutant deficient in the plastid Ndh complex was kinetically different from that of the wild type, the cycle being slower in the former leaves. We conclude that the Ndh complex is required for rapid electron cycling around PS I.During oxygenic photosynthesis, photosystem (PS) II and PS I cooperate to achieve a linear electron flow from H 2 O to NADP ϩ and to generate a transmembrane proton gradient driving ATP synthesis. However, ATP can also be produced by the sole PS I through cyclic electron transfer reactions (Arnon, 1959). This mechanism enables the generation of a proton gradient across the thylakoid membrane without NADP reduction by rerouting electrons of reduced PS I acceptors toward the intersystem carriers. Cyclic and linear electron transfers share a common sequence of electron carriers, namely the plastoquinone (PQ) pool, cytochrome b 6 /f complex, and plastocyanin (for review, see Fork and Herbert, 1993; Bendall and Manasse, 1995). This alternative electron flow has been shown to occur in vivo in cyanobacteria (Carpentier et al., 1984), in algae (Maxwell and Biggins, 1976; Ravenel et al., 1994), and in bundle sheath cells of C 4 plants (Herbert et al., 1990; Asada et al., 1993). In cyanobacteria, cyclic electron flow around PS I has been shown to provide extra ATP for different cellular processes, e.g. adaptation to salt stress conditions (Jeanjean et al., 1993). In the bundle sheath cell chloroplasts of C 4 plants, PS II is low or undetectable (Woo et al., 1970) and ATP supply is totally dependent upon PS I-mediated cyclic electron transport (Leegood et al., 1981).In C 3 plants, PS I-driven cyclic electron flow has been studied mainly in vitro on isolated chloroplasts or thylakoids with addition of artificial cofactors or reduced ferredoxi...

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Photosynthetic electron transport in the bundle sheath of maize

Cited by 31 publications

References 19 publications

Differential expression of plastome-encoded ndh genes in mesophyll and bundle-sheath chloroplasts of the C4 plant Sorghum bicolor indicates that the complex I-homologous NAD(P)H-plastoquinone oxidoreductase is involved in cyclic electron transport

Differential expression of plastome-encoded ndh genes in mesophyll and bundle-sheath chloroplasts of the C4 plant Sorghum bicolor indicates that the complex I-homologous NAD(P)H-plastoquinone oxidoreductase is involved in cyclic electron transport

Cyclic Electron Flow around Photosystem I in C3 Plants. In Vivo Control by the Redox State of Chloroplasts and Involvement of the NADH-Dehydrogenase Complex

Cyclic Electron Flow around Photosystem I in C3Plants. In Vivo Control by the Redox State of Chloroplasts and Involvement of the NADH-Dehydrogenase Complex

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